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Imaging the Centromedian Thalamic Nucleus Using Quantitative Susceptibility Mapping UC Berkeley UC Berkeley Previously Published Works Title Imaging the Centromedian Thalamic Nucleus Using Quantitative Susceptibility Mapping. Permalink https://escholarship.org/uc/item/7pm0m9bk Authors Li, Jun Li, Yufei Gutierrez, Lorenzo et al. Publication Date 2019 DOI 10.3389/fnhum.2019.00447 Peer reviewed eScholarship.org Powered by the California Digital Library University of California BRIEF RESEARCH REPORT published: 09 January 2020 doi: 10.3389/fnhum.2019.00447 Imaging the Centromedian Thalamic Nucleus Using Quantitative Susceptibility Mapping Jun Li 1†, Yufei Li 2†, Lorenzo Gutierrez 2, Wenying Xu 1, Yiwen Wu 3, Chunlei Liu 4,5, Dianyou Li 1, Bomin Sun 1, Chencheng Zhang 1* and Hongjiang Wei 2* 1Department of Functional Neurosurgery, Ruijin Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, China, 2Institute for Medical Imaging Technology, School of Biomedical Engineering, Shanghai Jiao Tong University, Shanghai, China, 3Department of Neurology, Ruijin Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, Edited by: China, 4Department of Electrical Engineering and Computer Sciences, University of California, Berkeley, Berkeley, CA, United 5 Adolfo Ramirez-Zamora, States, Helen Wills Neuroscience Institute, University of California, Berkeley, Berkeley, CA, United States University of Florida Health, United States The centromedian (CM) nucleus is an intralaminar thalamic nucleus that is considered as Reviewed by: a potentially effective target of deep brain stimulation (DBS) and ablative surgeries for the Wolf-Julian Neumann, Charité Medical University of Berlin, treatment of multiple neurological and psychiatric disorders. However, the structure of Germany CM is invisible on the standard T1- and T2-weighted (T1w and T2w) magnetic resonance Zhijiang Wang, Peking University Sixth Hospital, images, which hamper it as a direct DBS target for clinical applications. The purpose of China the current study is to demonstrate the use of quantitative susceptibility mapping (QSM) *Correspondence: technique to image the CM within the thalamic region. Twelve patients with Parkinson’s Chencheng Zhang disease, dystonia, or schizophrenia were included in this study. A 3D multi-echo gradient [email protected] Hongjiang Wei recalled echo (GRE) sequence was acquired together with T1w and T2w images on a [email protected] 3-T MR scanner. The QSM image was reconstructed from the GRE phase data. Direct †These authors have contributed visual inspection of the CM was made on T1w, T2w, and QSM images. Furthermore, equally to this work the contrast-to-noise ratios (CNRs) of the CM to the adjacent posterior part of thalamus Specialty section: on T1w, T2w, and QSM images were compared using the one-way analysis of variance This article was submitted to Brain Imaging and Stimulation, a section of (ANOVA) test. QSM dramatically improved the visualization of the CM nucleus. Clear the journal Frontiers in Human delineation of CM compared to the surroundings was observed on QSM but not on T1w Neuroscience and T2w images. Statistical analysis showed that the CNR on QSM was significantly Received: 17 September 2019 higher than those on T1w and T2w images. Taken together, our results indicate that Accepted: 05 December 2019 QSM is a promising technique for improving the visualization of CM as a direct targeting Published: 09 January 2020 for DBS surgery. Citation: Li J, Li Y, Gutierrez L, Xu W, Wu Y, Keywords: deep brain stimulation, direct targeting, gradient recalled echo, quantitative susceptibility mapping, Liu C, Li D, Sun B, Zhang C and Wei centromedian nucleus H (2020) Imaging the Centromedian Thalamic Nucleus Using Quantitative Susceptibility Mapping. Abbreviations: CM, centromedian nucleus; CNR, contrast-to-noise ratio; DBS, deep brain stimulation; GRE, gradient Front. Hum. Neurosci. 13:447. recalled echo; MRI, magnetic resonance imaging; QSM, quantitative susceptibility mapping; T1w, T1-weighted; T2w, doi: 10.3389/fnhum.2019.00447 T2-weighted. Frontiers in Human Neuroscience| www.frontiersin.org 1 January 2020 | Volume 13 | Article 447 Li et al. Imaging the Centromedian Nucleus INTRODUCTION accurate structural delineation (Liu et al., 2015). QSM has been clinically used to assess important tissue functions and disease The centromedian nucleus (CM) or centromedian–parafasicular (Wang et al., 2017), and recently it has been demonstrated nucleus complex, located in the caudal intralaminar thalamic for improving the depiction of DBS target structures with nuclei, has been reported to be a potentially effective target iron-rich nucleus (paramagnetic), e.g., the subthalamic nucleus for deep brain stimulation (DBS) or ablative surgeries for the (Liu et al., 2013; Alkemade et al., 2017) and the globus pallidus treatment of various neurological and psychiatric diseases, internus (Wei et al., 2019), with the surrounding white matters e.g., Parkinson’s disease, Tourette syndrome, generalized (diamagnetic). The thalamus contains different subregions that epilepsy, and intractable neuropathic pain (Ilyas et al., 2019). are known to have various iron deposits and different degrees However, the surgeries targeting CM still relied on the indirect of myelinated white matters (Morris et al., 1992; Zhang et al., targeting method by registering a normalized atlas to the patient’s 2018), which indicates that QSM, by using the susceptibility magnetic resonance imaging (MRI) data and then the CM differences existing between substructures, may be a proper coordinates are used for target localization (Krauss et al., 2002; imaging technique to identify CM. Kim et al., 2017; Sharma et al., 2017). This indirect targeting The aim of this study is to examine whether QSM could method may lead to suboptimal targeting since significant delineate the CM nucleus from its adjacent thalamic structures variations exist in brain structures between patients, and this and thus generate a direct visualization of the CM. variation causes unpredictable registration errors (Kennedy et al., 1998) and may sub-optimize treatment effect and increase MATERIALS AND METHODS the rate of surgical complications and adverse side effects (Chan et al., 2009). Human Subjects Direct targeting can improve the targeting accuracy in certain Twelve patients (six males and six females, mean age aspects as revealed by some studies (Tonge et al., 2016; Fenoy 41.8 ± 21.2 years old) with Parkinson’s disease (n = 5, mean and Schiess, 2018). Direct targeting requires that the anatomical age 61.0 ± 16.6), dystonia (n = 4, mean age 32.8 ± 8.6), or locations can be visible on certain image contrast. However, schizophrenia (n = 3, mean age 21.7 ± 10.3) were included as direct visualization of the CM nucleus using the standard T1w convenient samples in this study. Demographic information and T2w MRI sequences is challenging. On one hand, the volume collection and neuroradiological investigation were performed of the CM is small (smaller than 10 mm in most dimensions; by specialized movement disorder neurologists or psychiatrists. Ilyas et al., 2019). On the other hand, the contrast between The study was approved by the ethics committee of Ruijin the CM nucleus and its surrounding thalamic structures is Hospital, School of Medicine, Shanghai Jiao Tong University. pretty low. The absence of an imaging technique for direct All subjects provided written consent in accordance with the visualization of CM hampers the targeting accuracy of CM for Declaration of Helsinki. DBS surgery. Some researchers have made considerable efforts to improve Data Acquisition the individualized depiction of thalamic substructures. Lemaire Imaging was performed on a 3.0-T MR scanner equipped with et al.(2010) reported that high-resolution T1w images could be a 24-channel head coil. Each subject lay supine with their head used to image the substructures of the thalamus, which were very snugly fixed with foam pads. The subject was asked to keep still as comparable to myelin-stained histologic sections. However, the long as possible. 3D T1w and axial T2w images were acquired. A scan time for the protocol was approximately 14 h, which is not multi-echo GRE sequence was also performed. Detailed imaging suitable for routine clinical scans. Kanowski et al.(2010) showed parameters, including the time of repetition, time of echo, field that the CM is identifiable in a reasonable measurement time of view, voxel size, and total duration of scanning for the three of 13–26 min with two-dimensional high-resolution proton- imaging modalities, are summarized in Table 1. attenuation-weighted images at 3 T. However, only a few slices in axial plane covering the localized areas were acquired, which Image Processing still challenges targeting localization when using the surgical QSM images were reconstructed from GRE phase data. The planning software involving the 3D image registration procedure. details of QSM processing has been documented in the previous Bender et al.(2011) demonstrated that the CM could be roughly articles (Wei et al., 2015, 2017). In brief, three major steps identified by optimized 3D MPRAGE protocol, which would take were taken for the reconstruction of the QSM image. First, about 20 min to be acquired; however, clear discrimination of all the phase images of GRE were unwrapped using a Laplacian- thalamic substructures were not achievable. If anatomic imaging- based phase unwrapping. Afterward, the magnitude images were based targeting methods can be further improved, the accuracy used to extract
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